Genetic analyses reveal population structure and recent decline in leopards (Panthera pardus fusca) across the Indian subcontinent

Abstract

Background: Large carnivores maintain the stability and functioning of ecosystems. Currently, many carnivore species face declining population sizes due to natural and anthropogenic pressures. The leopard, Panthera pardus, is probably the most widely distributed and highly adaptable large felid globally, still persisting in most of its historic range. However, we lack subspecies-level data on country or regional scale on population trends, as ecological monitoring approaches are difficult to apply on such wide-ranging species. We used genetic data from leopards sampled across the Indian subcontinent to investigate population structure and patterns of demographic decline.

Methods: We collected faecal samples from the Terai-Arc landscape of northern India and identified 56 unique individuals using a panel of 13 microsatellite markers. We merged this data with already available 143 leopard individuals and assessed genetic structure at country scale. Subsequently, we investigated the demographic history of each identified subpopulations and compared genetic decline analyses with countrywide local extinction probabilities.

Results: Our genetic analyses revealed four distinct subpopulations corresponding to Western Ghats, Deccan Plateau-Semi Arid, Shivalik and Terai region of the north Indian landscape, each with high genetic variation. Coalescent simulations with microsatellite loci revealed a possibly human-induced 75-90% population decline between ∼120-200 years ago across India. Population-specific estimates of genetic decline are in concordance with ecological estimates of local extinction probabilities in these subpopulations obtained from occupancy modeling of the historic and current distribution of leopards in India.

Conclusions: Our results confirm the population decline of a widely distributed, adaptable large carnivore. We re-iterate the relevance of indirect genetic methods for such species in conjunction with occupancy assessment and recommend that detailed, landscape-level ecological studies on leopard populations are critical to future conservation efforts. Our approaches and inference are relevant to other widely distributed, seemingly unaffected carnivores such as the leopard.

Keywords: Carnivore conservation; Demographic history; Endangered species; Genetic variation; Leopardphylogeography; Population subdivision.

Figure 1. Genetic sampling and leopard population structure across the Indian subcontinent with forest cover map and leopard sampling locations used in this study.

The map also shows the inferred biogeographic leopard habitats based on genetic structure, as found in this study and corroborative leopard genetic clusters indicated by program STRUCTURE (based on 13 microsatellite loci).

Figure 2. Demographic history of Indian leopards (Panthera pardus fusca).

A, C, E and G show the posterior distributions for leopard population size changes for different subpopulations, based on 13 microsatellite loci using Storz and Beaumont approach. The dashed and solid lines represent posterior distributions of ancestral and present effective population sizes. The priors are represented by the dotted line. B, D, F, and H represent the posterior distribution for the time since the leopard population decline started for corresponding subpopulations. The priors are shown by the dotted lines.

Figure 3. Patterns of leopard occurrence in India based on the analysis of questionnaire surveys.

The map shows a gradient of estimated cell-wise occupancy probabilities created through spatial kriging.